Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex

Abstract

We have studied vertical synaptic pathways in two cytoarchitectonically distinct areas of rat neocortex--the granular primary somatosensory (SI) area and the agranular primary motor (MI) area--and tested their propensity to generate long-term potentiation (LTP), long-term depression (LTD), and related forms of synaptic plasticity. Extracellular and intracellular responses were recorded in layer II/III of slices in vitro while stimulating in middle cortical layers (in or around layer IV). Under control conditions, 5 Hz theta-burst stimulation produced LTP in the granular area, but not in the agranular area. Agranular cortex did generate short-term potentiation that decayed within 20 min. Varying the inter-burst frequency from 2 Hz to 10 Hz reliably yielded LTP of 21–34% above control levels in granular cortex, but no lasting changes were induced in agranular cortex. However, the agranular cortex was capable of generating LTP if a GABAA receptor antagonist was applied locally at the recording site during the induction phase. In contrast to LTP, an identical form of homosynaptic LTD could be induced in both granular and agranular areas by applying low frequency stimulation (1 Hz for 15 min) to the middle layers. Under control conditions, both LTP and LTD were synapse- specific; theta-burst or low-frequency stimulation in the vertical pathway did not induce changes in responses to stimulation of a layer II/III horizontal pathway. Application of the NMDA receptor antagonist D-2-amino-5-phosphonovaleric acid (AP5) blocked the induction of both LTP and LTD in granular and agranular cortex. In the presence of AP5, low-frequency conditioning stimuli yielded a short-term depression in both areas that decayed within 10–15 min. Nifedipine, which blocks L- type, voltage-sensitive calcium channels, slightly depressed the magnitudes of LTP and LTD but did not abolish them. Synaptic responses evoked during theta-burst stimulation were strikingly different in granular and agranular areas. Responses in granular cortex were progressively facilitated during each sequence of 10 theta-bursts, and from sequence-to-sequence; in contrast, responses in agranular cortex were stable during an entire theta-burst tetanus. The results suggest that vertical pathways in primary somatosensory cortex and primary motor cortex express several forms of synaptic plasticity. They were equally capable of generating LTD, but the pathways in somatosensory cortex much more reliably generated LTP, unless inhibition was reduced. LTP may be more easily produced in sensory cortex because of the pronounced synaptic facilitation that occurs there during repetitive stimulation of the induction phase.

Neuromodulatory Neurotransmitters Influence LTP-Like Plasticity in Human Cortex: A Pharmaco-TMS Study

“…This is in line with experiments in preparations of rat neocortex demonstrating that in contrast to LTP induction in primary somatosensory cortex, LTP induction in M1 does not show postsynaptic potential facilitation during repetitive burst stimulation in the LTP induction phase, and stable LTP can be obtained only under conditions of local disinhibition (Castro-Alamancos et al, 1995).…”

Activity-Dependent Regulation of NMDAR1 Immunoreactivity in the Developing Visual Cortex

“…NMDA receptor-dependent LTP and LTD can be evoked in slices of cat and rat visual cortex and rat somatosensory cortex from young animals. At older ages and in adulthood, LTP and LTD can no longer be induced in layer 4 but can still be induced in layers 2/3 (Komatsu et al, 1988;Perkins and Teyler, 1988;Kirkwood and Bear, 1994;Castro-Alamancos et al, 1995;Crair and Malenka, 1995;Dudek and Friedlander, 1996;Isaac et al, 1997; for review, see Bear and Malenka, 1994). Changing levels of NMDAR1 seen here may partially account for the changing capacity for LTP and LTD during development.…”

Deleterious Effects of a Low Amount of Ethanol on LTP-Like Plasticity in Human Cortex

“…In slice preparations of rat motor cortex (M1), LTP induction depends on disinhibition by application of a synaptic GABAAR antagonist and can be disrupted by NMDAR blockade (Aroniadou and Keller, 1995;Castro-Alamancos et al, 1995;Fritsch et al, 2010;Hess et al, 1996). At the systems level of human M1, LTP-like plasticity, indexed by a long-term increase in motor-evoked potential (MEP) amplitude, can be induced by paired associative stimulation (PAS LTP ) (Cooke and Bliss, 2006;Müller-Dahlhaus et al, 2010;Stefan et al, 2002;Stefan et al, 2000;Ziemann et al, 2004).…”